Cross-regional coordination of activity in the human brain during autobiographical self-referential processing.

For the human brain to operate, populations of neurons across anatomical structures must coordinate their activity within milliseconds. To date, our understanding of such interactions has remained limited. We recorded directly from the hippocampus (HPC), posteromedial cortex (PMC), ventromedial/orbital prefrontal cortex (OFC), and the anterior nuclei of the thalamus (ANT) during two experiments of autobiographical memory processing that are known from decades of neuroimaging work to coactivate these regions. In 31 patients implanted with intracranial electrodes, we found that the presentation of memory retrieval cues elicited a significant increase of low frequency (LF < 6 Hz) activity followed by cross-regional phase coherence of this LF activity before select populations of neurons within each of the four regions increased high-frequency (HF > 70 Hz) activity. The power of HF activity was modulated by memory content, and its onset followed a specific temporal order of ANT→HPC/PMC→OFC. Further, we probed cross-regional causal effective interactions with repeated electrical pulses and found that HPC stimulations cause the greatest increase in LF-phase coherence across all regions, whereas the stimulation of any region caused the greatest LF-phase coherence between that particular region and ANT. These observations support the role of the ANT in gating, and the HPC in synchronizing, the activity of cortical midline structures when humans retrieve self-relevant memories of their past. Our findings offer a fresh perspective, with high temporal fidelity, about the dynamic signaling and underlying causal connections among distant regions when the brain is actively involved in retrieving self-referential memories from the past.

Causal Cortical and Thalamic Connections in the Human Brain.

The brain's functional architecture is intricately shaped by causal connections between its cortical and subcortical structures. Here, we studied 27 participants with 4864 electrodes implanted across the anterior, mediodorsal, and pulvinar thalamic regions, and the cortex. Using data from electrical stimulation procedures and a data-driven approach informed by neurophysiological standards, we dissociated three unique spectral patterns generated by the perturbation of a given brain area. Among these, a novel waveform emerged, marked by delayed-onset slow oscillations in both ipsilateral and contralateral cortices following thalamic stimulations, suggesting a mechanism by which a thalamic site can influence bilateral cortical activity. Moreover, cortical stimulations evoked earlier signals in the thalamus than in other connected cortical areas suggesting that the thalamus receives a copy of signals before they are exchanged across the cortex. Our causal connectivity data can be used to inform biologically-inspired computational models of the functional architecture of the brain.

Intracranial Recordings of the Human Orbitofrontal Cortical Activity during Self-Referential Episodic and Valenced Self-Judgments.

We recorded directly from the orbital (oPFC) and ventromedial (vmPFC) subregions of the orbitofrontal cortex (OFC) in 22 (9 female, 13 male) epilepsy patients undergoing intracranial electroencephalography (iEEG) monitoring during an experimental task in which the participants judged the accuracy of self-referential autobiographical statements as well as valenced self-judgments (SJs). We found significantly increased high-frequency activity (HFA) in ∼13% of oPFC sites (10/18 subjects) and 16% of vmPFC sites (4/12 subjects) during both of these self-referential thought processes, with the HFA power being modulated by the content of self-referential stimuli. The location of these activated sites corresponded with the location of fMRI-identified limbic network. Furthermore, the onset of HFA in the vmPFC was significantly earlier than that in the oPFC in all patients with simultaneous recordings in both regions. In 11 patients with available depression scores from comprehensive neuropsychological assessments, we documented diminished HFA in the OFC during positive SJ trials among individuals with higher depression scores; responses during negative SJ trials were not related to the patients' depression scores. Our findings provide new temporal and anatomical information about the mode of engagement in two important subregions of the OFC during autobiographical memory and SJ conditions. Our findings from the OFC support the hypothesis that diminished brain activity during positive self-evaluations, rather than heightened activity during negative self-evaluations, plays a key role in the pathophysiology of depression.

Causal evidence for the processing of bodily self in the anterior precuneus.

To probe the causal importance of the human posteromedial cortex (PMC) in processing the sense of self, we studied a rare cohort of nine patients with electrodes implanted bilaterally in the precuneus, posterior cingulate, and retrosplenial regions with a combination of neuroimaging, intracranial recordings, and direct cortical stimulations. In all participants, the stimulation of specific sites within the anterior precuneus (aPCu) caused dissociative changes in physical and spatial domains. Using single-pulse electrical stimulations and neuroimaging, we present effective and resting-state connectivity of aPCu hot zone with the rest of the brain and show that they are located outside the boundaries of the default mode network (DMN) but connected reciprocally with it. We propose that the function of this subregion of the PMC is integral to a range of cognitive processes that require the self's physical point of reference, given its location within a spatial environment.

Benefits of deep learning classification of continuous noninvasive brain-computer interface control.

Objective. Noninvasive brain-computer interfaces (BCIs) assist paralyzed patients by providing access to the world without requiring surgical intervention. Prior work has suggested that EEG motor imagery based BCI can benefit from increased decoding accuracy through the application of deep learning methods, such as convolutional neural networks (CNNs).Approach. Here, we examine whether these improvements can generalize to practical scenarios such as continuous control tasks (as opposed to prior work reporting one classification per trial), whether valuable information remains latent outside of the motor cortex (as no prior work has compared full scalp coverage to motor only electrode montages), and the existing challenges to the practical implementation of deep-learning based continuous BCI control.Main results. We report that: (1) deep learning methods significantly increase offline performance compared to standard methods on an independent, large, and longitudinal online motor imagery BCI dataset with up to 4-classes and continuous 2D feedback; (2) our results suggest that a variety of neural biomarkers for BCI, including those outside the motor cortex, can be detected and used to improve performance through deep learning methods, and (3) tuning neural network output will be an important step in optimizing online BCI control, as we found the CNN models trained with full scalp EEG also significantly reduce the average trial length in a simulated online cursor control environment.Significance. This work demonstrates the benefits of CNNs classification during BCI control while providing evidence that electrode montage selection and the mapping of CNN output to device control will be important design choices in CNN based BCIs.

Continuous sensorimotor rhythm based brain computer interface learning in a large population.

Brain computer interfaces (BCIs) are valuable tools that expand the nature of communication through bypassing traditional neuromuscular pathways. The non-invasive, intuitive, and continuous nature of sensorimotor rhythm (SMR) based BCIs enables individuals to control computers, robotic arms, wheel-chairs, and even drones by decoding motor imagination from electroencephalography (EEG). Large and uniform datasets are needed to design, evaluate, and improve the BCI algorithms. In this work, we release a large and longitudinal dataset collected during a study that examined how individuals learn to control SMR-BCIs. The dataset contains over 600 hours of EEG recordings collected during online and continuous BCI control from 62 healthy adults, (mostly) right hand dominant participants, across (up to) 11 training sessions per participant. The data record consists of 598 recording sessions, and over 250,000 trials of 4 different motor-imagery-based BCI tasks. The current dataset presents one of the largest and most complex SMR-BCI datasets publicly available to date and should be useful for the development of improved algorithms for BCI control.

Frontolimbic alpha activity tracks intentional rest BCI control improvement through mindfulness meditation.

Brain-computer interfaces (BCIs) are capable of translating human intentions into signals controlling an external device to assist patients with severe neuromuscular disorders. Prior work has demonstrated that participants with mindfulness meditation experience evince improved BCI performance, but the underlying neural mechanisms remain unclear. Here, we conducted a large-scale longitudinal intervention study by training participants in mindfulness-based stress reduction (MBSR; a standardized mind-body awareness training intervention), and investigated whether and how short-term MBSR affected sensorimotor rhythm (SMR)-based BCI performance. We hypothesize that MBSR training improves BCI performance by reducing mind wandering and enhancing self-awareness during the intentional rest BCI control, which would mainly be reflected by modulations of default-mode network and limbic network activity. We found that MBSR training significantly improved BCI performance compared to controls and these behavioral enhancements were accompanied by increased frontolimbic alpha activity (9-15 Hz) and decreased alpha connectivity among limbic network, frontoparietal network, and default-mode network. Furthermore, the modulations of frontolimbic alpha activity were positively correlated with the duration of meditation experience and the extent of BCI performance improvement. Overall, these data suggest that mindfulness allows participant to reach a state where they can modulate frontolimbic alpha power and improve BCI performance for SMR-based BCI control.

Mindfulness Improves Brain-Computer Interface Performance by Increasing Control Over Neural Activity in the Alpha Band.

Brain-computer interfaces (BCIs) are promising tools for assisting patients with paralysis, but suffer from long training times and variable user proficiency. Mind-body awareness training (MBAT) can improve BCI learning, but how it does so remains unknown. Here, we show that MBAT allows participants to learn to volitionally increase alpha band neural activity during BCI tasks that incorporate intentional rest. We trained individuals in mindfulness-based stress reduction (MBSR; a standardized MBAT intervention) and compared performance and brain activity before and after training between randomly assigned trained and untrained control groups. The MBAT group showed reliably faster learning of BCI than the control group throughout training. Alpha-band activity in electroencephalogram signals, recorded in the volitional resting state during task performance, showed a parallel increase over sessions, and predicted final BCI performance. The level of alpha-band activity during the intentional resting state correlated reliably with individuals' mindfulness practice as well as performance on a breath counting task. Collectively, these results show that MBAT modifies a specific neural signal used by BCI. MBAT, by increasing patients' control over their brain activity during rest, may increase the effectiveness of BCI in the large population who could benefit from alternatives to direct motor control.

Effects of Long-Term Meditation Practices on Sensorimotor Rhythm-Based Brain-Computer Interface Learning.

Sensorimotor rhythm (SMR)-based brain-computer interfaces (BCIs) provide an alternative pathway for users to perform motor control using motor imagery. Despite the non-invasiveness, ease of use, and low cost, this kind of BCI has limitations due to long training times and BCI inefficiency-that is, the SMR BCI control paradigm may not work well on a subpopulation of users. Meditation is a mental training method to improve mindfulness and awareness and is reported to have positive effects on one's mental state. Here, we investigated the behavioral and electrophysiological differences between experienced meditators and meditation naïve subjects in one-dimensional (1D) and two-dimensional (2D) cursor control tasks. We found numerical evidence that meditators outperformed control subjects in both tasks (1D and 2D), and there were fewer BCI inefficient subjects in the meditator group. Finally, we also explored the neurophysiological difference between the two groups and showed that the meditators had a higher resting SMR predictor, more stable resting mu rhythm, and a larger control signal contrast than controls during the task.